Large-scale heterospecific segregation distortion in Populus revealed by a dense genetic map

Abstract

We report the most complete genetic map to have been constructed for the genus Populus. This map includes 544 markers mapped onto 19 linkage groups, equivalent to the Populus chromosome number, with all markers displaying internally consistent linkage patterns. We estimate the genome length to be between 2,300 and 2,500 cM, based both on the observed number of crossovers in the maternal haplotypes, as well as the total observed map length. Genome coverage was estimated to be greater than 99.9% at 20 cM per marker. We did not detect obvious recombination repression in the maternal tree (a hybrid of Populus trichocarpa Hooker x P. deltoides Marsh.) compared to the paternal tree (pure P. deltoides). Finally, most markers exhibiting segregation distortion were derived from the donor parent in this backcross, and generally occurred in large contiguous blocks on two linkage groups. We hypothesize that divergent selection has occurred on chromosomal scales among the parental species used to create this pedigree, and explore the evolutionary implications of this observation. This genetic linkage map provides the most comprehensive view of the Populus genome reported to date and will prove invaluable for future inquiries into the structural and functional genomics, evolutionary biology, and genetic improvement of this ecologically important model species.

A dense linkage map of hybrid cottonwood (Populus fremontii × P. angustifolia) contributes to long-term ecological research and comparison mapping in a model forest tree

“…Initial screening was conducted with both parents and six progeny, and loci that appeared to be segregating in both parents were selected for mapping. SSR amplification and genotyping was performed as described elsewhere (Yin et al, 2004), except loci were analyzed on an ABI3730 automated capillary electrophoresis instrument, and amplification was performed with 10 pmol fluorescein 12-dUTP (Roche Diagnostics, Indianapolis, IN, USA), rather than end-labeled primers.…”

The obscure events contributing to the evolution of an incipient sex chromosome in Populus: a retrospective working hypothesis

“…Genome organization and chromosome structure have been conserved among Populus and Salix species (Berlin et al 2010), and comparisons among Populus and Salix orthologous genes suggest that both genera share this whole-genome duplication event that predated the speciation event (Tuskan et al 2006). Comparative mapping reveals near-complete marker colinearity in pedigrees established from multiple species within Populus and among members of Salix (Cervera et al 2001;Hanley et al 2006;Yin et al 2004aYin et al , 2008Berlin et al 2010) (Table 1). Interestingly, Berlin et al (2010) identified a large region of segregation distortion on linkage group XIX that corresponds to a similar region in chromosome XIX in Populus .…”

“…Dioecy in Populus is strongly genetically controlled, and a region of the genome located on chromosome XIX appears to contain a gene (genes) that controls gender determination, though there are noted examples of gender reversion and hermaphroditic plants in most species (Rottenberg et al 2000;Markussen et al 2007;Gaudet et al 2008;Pakull et al 2009Pakull et al , 2011Paolucci et al 2010). The peritelomeric region on chromosome XIX in female Populus trichocarpa genotypes contains approximately 1 Mb of DNA that is not found in male genotypes and appears to have a region of suppressed and/or reduced recombination that extends 3-4 Mb beyond the hemizygous segment in females (Yin et al 2004a). …”

“…Second, suppressed recombination in this region was only observed in the female parent. Finally, distorted segregation ratios have been observed in the maternal genotypes of several mapping populations in Populus (Yin et al 2004a). However, the gender-determining locus has not been resolved into an individual gene (genes) yet.…”

Transmission ratio distortion in Arabidopsis lyrata: effects of population divergence and the S-locus

“…Epistatic interactions between two or more loci (DobzhanskyMuller incompatibilities) or chromosomal differentiation related to divergence may give rise to transmission ratio distortion in crosses between species or subspecies (reviewed in Fishman and Willis, 2001). Severe transmission ratio distortion has been found in progeny of both interspecific crosses (Fishman and Willis, 2001;Myburg et al, 2004;Yin et al, 2004) and intraspecific crosses between diverged populations (Hall and Willis, 2005;Tö rjék et al, 2006). Earlier studies have generally reported a larger transmission ratio distortion in interspecific crosses than in intraspecific crosses (Zamir and Tadmor, 1986;Jenczewski et al, 1997).…”